Central neural coding of sky polarization in insects.

Abstract

Many animals rely on a sun compass for spatial orientation and long-range navigation. In addition to the Sun, insects also exploit the polarization pattern and chromatic gradient of the sky for estimating navigational directions. Analysis of polarization-vision pathways in locusts and crickets has shed first light on brain areas involved in sky compass orientation. Detection of sky polarization relies on specialized photoreceptor cells in a small dorsal rim area of the compound eye. Brain areas involved in polarization processing include parts of the lamina, medulla and lobula of the optic lobe and, in the central brain, the anterior optic tubercle, the lateral accessory lobe and the central complex. In the optic lobe, polarization sensitivity and contrast are enhanced through convergence and opponency. In the anterior optic tubercle, polarized-light signals are integrated with information on the chromatic contrast of the sky. Tubercle neurons combine responses to the UV/green contrast and e-vector orientation of the sky and compensate for diurnal changes of the celestial polarization pattern associated with changes in solar elevation. In the central complex, a topographic representation of e-vector tunings underlies the columnar organization and suggests that this brain area serves as an internal compass coding for spatial directions.

Sensory basis of polarization vision in the locust S. gregaria. (a) Pattern of polarized light of the blue sky. Electrical field vectors (e-vectors, double arrows) are arranged along concentric circles around the Sun (yellow). Direct sunlight is unpolarized. The degree of polarization in the sky increases gradually to a maximum of about 0.75 along a circle at 90° from the Sun. (b) Polarization-sensitive dorsal rim area (DRA) in the left compound eye of a locust, arrangement of ommatidia and organization of a DRA ommatidium. In each DRA ommatidium, the microvilli of photoreceptor cell 7 are oriented perpendicularly to the microvilli of photoreceptors 1, 2, 5, 6 and 8. Microvilli of photoreceptors 3 and 4 are irregular. a, anterior. (c,d) Yaw-torque responses of tethered flying locusts under a slowly rotating dorsal polarizer. Each histogram shows average yaw torques from six 180° rotations of the polarizer divided in 5° bins. The animal in (c) shows strong polarotaxis. After painting the DRAs of the eyes black (d), polarotaxis is abolished. (b) From Homberg & Paech [] and (c,d) from Mappes & Homberg [].

Polarization-sensitive POL1 neuron in the brain of the cricket Gryllus campestris. (a) Morphology of POL1. The neuron has dendritic arborizations in the dorsal medulla (Me) and an axonal projection to the contralateral medulla. Side branches are in the accessory medulla (AMe) of both brain hemispheres. S, soma. Scale bar, 250 µm. Reprinted from Labhart & Petzold [], with permission from Birkhäuser Verlag. (b) Intracellular recording from POL1 in the ipsilateral optic lobe. The neuron shows polarization opponency when the animal is stimulated dorsally through a polarizer rotating from 360° to 0° and back. (c) The receptive field of POL1 (shaded area) extends through an area of about 60° in the contralateral (c) dorsal field of view. a, anterior; i, ipsilateral; p, posterior. (b,c) Reprinted from Wehner & Labhart [], with permission from Cambridge University Press. (d) Histogram of e-vector tunings from 142 recordings from POL1 neurons. Three physiological types can be distinguished with Φmax orientations around 10°, 60° and 130° with respect to the longitudinal axis of the animal. Reprinted from Labhart & Meyer [], with permission from Elsevier.

Polarization–vision pathway to the central complex in the brain of the locust, as revealed through tracer injections into the dorsal rim area of the eye, into the dorsal rim of the medulla (DMe), into the anterior optic tubercle (AOTu) and through dye injection into single neurons of the central body. Central processing stages for polarized light include the dorsal rim of the lamina and medulla (DLa and DMe), layer 1 of the anterior lobe of the lobula (ALo1), the lower unit of the AOTu (AOTu-LU), the median olive (MO) and lateral triangle (LT) of the lateral accessory lobe (LAL), and the lower division of the central body (CBL). Ca and P, calyx and pedunculus of the mushroom body; La, lamina; Me, medulla; PB, protocerebral bridge. Scale bar, 200 µm. Adapted from Träger et al. [].

Polarization-sensitive neurons of the anterior optic tubercle in the locust brain. (a,b) Morphology of two types of polarization-sensitive commissural neurons, termed LoTu1 and TuTu1, that connect the lower units of the anterior optic tubercles (AOTu-LU) of both hemispheres. LoTu1 has additional ramifications in the ventralmost layer 1 of the anterior lobe of the lobula (ALo) of both hemispheres. AOT, anterior optic tract; CB, central body; MB, mushroom body; AOTu-UU, upper unit of the anterior optic tubercle. Scale bars, 200 µm. (c–e) Responses of a TuTu1 neuron to different orientations of polarized blue (470 nm) light in the zenith (c) and different azimuthal positions of a green (530 nm; d) and a UV (350 nm; e) light spot. Background spiking activity is indicated by the red circles. Black bars show preference angles (ΦmaxPOL, Φmaxgreen, ΦmaxUV) of the neuron to the different stimuli. (f) Absolute angular differences ΔΦmax between ΦmaxPOL and Φmaxgreen from all recordings plotted against time of day of the experiments reveal diurnal changes in the difference angles. Celestial ΔΦmax functions strongly depend on geographical coordinates and are fitted to the data for coordinates of Marburg, Germany (blue line) and northern Africa (red line). (g) e-vector response plots for stimulation of both eyes (blue triangles), the ipsilateral eye (red squares) and the contralateral eye (green circles) show that polarization input to TuTu1 is strongly dominated by the ipsilateral eye. (a,b,g) From Pfeiffer et al. [] and (c–f) from Pfeiffer & Homberg [].

Proposed scheme of the polarization coding network in the locust central complex. Neurons at the input stage are shown in shades of blue, neurons at an intermediate stage in green and neurons at the output stage in shades of red. Polarization–vision information from the optic lobe (blue arrows) enters the lower division of the central body (CBL) via TuLAL1a/b neurons from the lower unit of the anterior optic tubercle (AOTu-LU). These neurons synapse in the lateral triangle (LT) and medial olive (MO) of the lateral accessory lobe (LAL) upon tangential TL2/3 neurons of the CBL. At the following intermediate stage, CL1 neurons (green) are candidates to transmit polarization–vision signals from the CBL to the contralateral hemisphere of the protocerebral bridge (PB). For clarity, only four of 16 neurons are shown. Via small axons, these neurons also provide a first, direct output pathway to a small region near the LT in the LAL (green asterisks). Neurons at the final output stage (TB1, CPU1; red) contribute to the topographic representation of e-vectors in the PB columns, illustrated for CPU1 neurons as double arrows above the PB. Whereas TB1 neurons project to the posterior optic tubercle (POTu), CPU1 cells and other columnar neurons target post-synaptic neurons in the LAL (red asterisks). CPU1 neurons (only two of 16 shown) receive additional input in the upper division of the central body (CBU). Based on data from Heinze & Homberg [,,], Pfeiffer et al. [], Vitzthum et al. [], Heinze et al. [] and Träger et al. [].